Occurrence of Antimicrobial Resistance in Indicator Bacteria and Campylobacter spp. Isolated from Commercial Raw-Meat-Based Food for Dogs and Cats in Belgium
Abstract
1. Introduction
2. Results
2.1. Sample Collection and Properties
2.2. Detection of Bacteria
Selective Isolation of Resistant Strains
2.3. Antimicrobial Susceptibility Results
2.4. Risk Factors
3. Discussion
3.1. The Prevalence of Indicator Bacteria and the Occurrence of AMR Patterns
3.2. Antimicrobial Resistance Patterns Observed
3.3. Risk Factors
3.4. Study Limitations and Future Research
4. Materials and Methods
4.1. Sampling Methods
4.2. Bacterial Isolation and Identification
4.2.1. E. coli Isolation
4.2.2. E. faecalis and E. faecium Isolation
4.2.3. Selective Isolation of Resistant Strains
4.2.4. Campylobacter spp. Isolation
4.3. Antimicrobial Susceptibility
4.4. Data Analysis
4.4.1. Statistical Methods
4.4.2. Risk Factors
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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| Antimicrobial Agent | Number of Strains with MIC (mg/L) and Tested Range | Wild-Type | Non-Wild-Type | |||||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 0.015 | 0.03 | 0.06 | 0.125 | 0.25 | 0.5 | 1 | 2 | 4 | 8 | 16 | 32 | 64 | 128 | 256 | 512 | [n] | [%] | [n] | [%] | |
| Amikacin | 45 | 0 | 0 | 0 | 0 | 0 | 45 | 100.0% | 0 | 0.0% | ||||||||||
| Gentamicin | 37 | 7 | 0 | 0 | 0 | 1 | 44 | 97.8% | 1 | 2.2% | ||||||||||
| Ampicillin | 2 | 10 | 14 | 2 | 0 | 17 | 28 | 62.2% | 17 | 37.8% | ||||||||||
| Azithromycin | 4 | 19 | 22 | 0 | 0 | 0 | 45 | 100.0% | 0 | 0.0% | ||||||||||
| Cefotaxime | 34 | 0 | 1 | 2 | 8 | 34 | 75.6% | 11 | 24.4% | |||||||||||
| Ceftazidime | 34 | 0 | 2 | 1 | 2 | 6 | 34 | 75.6% | 11 | 24.4% | ||||||||||
| Chloramphenicol | 42 | 0 | 0 | 3 | 42 | 93.3% | 3 | 6.7% | ||||||||||||
| Ciprofloxacin | 36 | 2 | 0 | 4 | 2 | 0 | 0 | 0 | 0 | 1 | 38 | 84.4% | 7 | 15.6% | ||||||
| Nalidixic Acid | 39 | 1 | 0 | 1 | 4 | 40 | 88.9% | 5 | 11.1% | |||||||||||
| Colistin | 43 | 0 | 0 | 0 | 2 | 43 | 95.6% | 2 | 4.4% | |||||||||||
| Meropenem | 44 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 45 | 100.0% | 0 | 0.0% | ||||||
| Sulfamethoxazole | 15 | 15 | 2 | 1 | 0 | 0 | 12 | 33 | 73.3% | 12 | 26.7% | |||||||||
| Trimethoprim | 17 | 21 | 0 | 0 | 0 | 0 | 7 | 38 | 84.4% | 7 | 15.6% | |||||||||
| Tetracycline | 31 | 0 | 0 | 0 | 14 | 31 | 68.9% | 14 | 31.1% | |||||||||||
| Tigecycline | 44 | 1 | 0 | 0 | 0 | 0 | 45 | 100.0% | 0 | 0.0% | ||||||||||
| Antimicrobial Agent | Number of Strains with MIC (mg/L) and Tested Range | Wild-Type | Non-Wild-Type | ||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 0.03 | 0.06 | 0.125 | 0.25 | 0.5 | 1 | 2 | 4 | 8 | 16 | 32 | 64 | 128 | [n] | [%] | [n] | [%] | |
| Ampicillin | 5 | 15 | 9 | 1 | 0 | 0 | 0 | 1 | 30 | 96.8% | 1 | 3.2% | |||||
| Chloramphenicol | 5 | 24 | 2 | 0 | 0 | 0 | 31 | 100.0% | 0 | 0.0% | |||||||
| Ciprofloxacin | 0 | 0 | 3 | 22 | 3 | 3 | 0 | 0 | 31 | 100.0% | 0 | 0.0% | |||||
| Daptomycin | 0 | 0 | 21 | 6 | 3 | 1 | 0 | 0 | 30 | 96.8% | 1 | 3.2% | |||||
| Erythromycin | 12 | 11 | 0 | 1 | 1 | 0 | 0 | 6 | 23 | 74.2% | 8 | 25.8% | |||||
| Gentamicin | 19 | 12 | 0 | 0 | 0 | 31 | 100.0% | 0 | 0.0% | ||||||||
| Linezolid | 0 | 4 | 26 | 1 | 0 | 0 | 0 | 0 | 31 | 100.0% | 0 | 0.0% | |||||
| Quinupristin/Dalfopristin | 1 | 2 | 0 | 1 | 14 | 13 | 0 | 0 | 3 | 9.7% | 28 | 90.3% | |||||
| Teicoplanin | 31 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 31 | 100.0% | 0 | 0.0% | |||||
| Vancomycin | 17 | 7 | 6 | 1 | 0 | 0 | 0 | 0 | 30 | 96.8% | 1 | 3.2% | |||||
| Tetracycline | 15 | 0 | 0 | 0 | 0 | 2 | 9 | 5 | 15 | 48.4% | 16 | 51.6% | |||||
| Tigecycline | 5 | 13 | 12 | 1 | 0 | 0 | 0 | 0 | 31 | 100.0% | 0 | 0.0% | |||||
| Antimicrobial Agent | Number of Strains with MIC (mg/L) and Tested Range | Wild-Type | Non-Wild-Type | ||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 0.03 | 0.06 | 0.125 | 0.25 | 0.5 | 1 | 2 | 4 | 8 | 16 | 32 | 64 | 128 | [n] | [%] | [n] | [%] | |
| Ampicillin | 2 | 8 | 10 | 1 | 1 | 0 | 0 | 1 | 21 | 91.3% | 2 | 8.7% | |||||
| Chloramphenicol | 7 | 14 | 0 | 1 | 1 | 0 | 22 | 95.7% | 1 | 4.3% | |||||||
| Ciprofloxacin | 0 | 1 | 3 | 4 | 6 | 7 | 2 | 0 | 21 | 91.3% | 2 | 8.7% | |||||
| Daptomycin | 0 | 1 | 1 | 9 | 12 | 0 | 0 | 0 | 23 | 100.0% | 0 | 0.0% | |||||
| Erythromycin | 12 | 6 | 2 | 1 | 0 | 0 | 0 | 2 | 20 | 87.0% | 3 | 13.0% | |||||
| Gentamicin | 21 | 2 | 0 | 0 | 0 | 23 | 100.0% | 0 | 0.0% | ||||||||
| Linezolid | 0 | 0 | 21 | 1 | 1 | 0 | 0 | 0 | 22 | 95.7% | 1 | 4.3% | |||||
| Quinupristin/Dalfopristin | 5 | 4 | 3 | 10 | 1 | 0 | 0 | 0 | 9 | 39.1% | 14 | 60.9% | |||||
| Teicoplanin | 22 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 23 | 100.0% | 0 | 0.0% | |||||
| Vancomycin | 18 | 3 | 2 | 0 | 0 | 0 | 0 | 0 | 23 | 100.0% | 0 | 0.0% | |||||
| Tetracycline | 16 | 0 | 0 | 0 | 0 | 1 | 2 | 4 | 16 | 69.6% | 7 | 30.4% | |||||
| Tigecycline | 3 | 8 | 10 | 2 | 0 | 0 | 0 | 0 | 23 | 100.0% | 0 | 0.0% | |||||
| Isolates | Antibiotic Resistance Profiles | No. of Antibiotic (Sub)-Class Resistances |
|---|---|---|
| E. coli | ||
| EC01 | CTX-CAZ-CIP-NAL-COL | 3 |
| EC02 | AMP-CHL-SXT-TET-TMP | 5 |
| EC03 | AMP-CTX-CAZ-CHL-CIP-NAL-TET-TMP | 6 |
| EC04 | AMP-SXT-TET-TMP | 4 |
| EC05 | AMP-CTX-CAZ-SXT-TET | 4 |
| EC06 | AMP-CTX-CAZ-SXT-TET | 4 |
| EC07 | AMP-CTX-SXT | 3 |
| EC08 | AMP-SXT-TMP | 3 |
| EC09 | GEN-AMP-CTX-CAZ-CIP-SXT-TET-TMP | 7 |
| EC10 | AMP-CTX-CAZ-TET | 3 |
| EC11 | AMP-CTX-CAZ-TET | 3 |
| EC12 | AMP-CTX-CAZ-CHL-SXT-TET-TMP | 6 |
| EC13 | AMP-CIP-NAL-SXT-TET-TMP | 5 |
| EC14 | CAZ-CIP-NAL-COL-SXT | 4 |
| E. faecalis | ||
| EFS1 | AMP-ERY-QD-TET | 3 * |
| E. faecium | ||
| EFM1 | CHL-ERY-LZD-QD-TET | 5 |
| EFM2 | AMP-CIP-ERY-QD-TET | 5 |
| E. coli (N = 45) | E. faecalis (N = 31) | E. faecium (N = 23) | Samples with MDR Indicator Strains (N = 15) | |||||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Variable | [N] | Present [n/N] | [%] | OR (95% CI) | p-Val | Present [n/N] | [%] | OR (95% CI) | p-Val | Present [n/N] | [%] | OR (95% CI) | p-Val | Detected [n/N] | [%] | OR (95% CI) | p-Val | |
| Production Location | Belgium | 17 | 17/17 | 100.0 | N/A | 0.279 | 8/17 | 47.1 | 0.42 (0.12–1.45) | 0.216 | 13/17 | 76.5 | 11.9 (2.83–50.25) | <0.001 | 6/17 | 35.3 | 1.36 (0.38–4.95) | 0.744 |
| Netherlands | 28 | 25/28 | 89.3 | 1.00 (ref) | - | 19/28 | 67.9 | 1.00 (ref) | - | 6/28 | 21.4 | 1.00 (ref) | 8/28 | 28.6 | 1.00 (ref) | |||
| Others | 5 | 3/5 | 60 | 0.18 (0.02–1.55) | 0.155 | 4/5 | 80.0 | 1.90 (0.18–19.48) | 1.000 | 4/5 | 80 | 14.67 (1.37–156.89) | 0.021 | 1/5 | 20 | 0.63 (0.60–6.49) | 1.000 | |
| Overall test | 0.032 | 0.320 | <0.001 | 0.905 | ||||||||||||||
| Muscle tissue | Present | 33 | 29/33 | 87.9 | 0.45 (0.05–4.01) | 0.650 | 18/33 | 54.6 | 0.37 (0.10–1.37) | 0.218 | 15/33 | 45.5 | 0.94 (0.29–3.03) | 1.000 | 12/33 | 36.4 | 2.68 (0.64–11.12) | 0.209 |
| Absent | 17 | 16/17 | 94.1 | 13/17 | 76.5 | 8/17 | 47.1 | 3/17 | 17.6 | |||||||||
| Offal | Present | 22 | 21/22 | 95.5 | 3.50 (0.36–33.82) | 0.368 | 14/22 | 63.6 | 1.13 (0.35–3.59) | 1.000 | 8/22 | 36.4 | 0.51 (0.16–1.55) | 0.264 | 5/22 | 22.7 | 0.53 (0.15–1.87) | 0.367 |
| Absent | 28 | 24/28 | 85.7 | 17/28 | 60.7 | 15/28 | 53.6 | 10/28 | 35.7 | |||||||||
| Bones | Present | 16 | 13/16 | 81.3 | 0.27 (0.04–1.81) | 0.311 | 11/16 | 68.8 | 1.54 (0.44–5.42) | 0.549 | 6/16 | 37.5 | 0.60 (0.18–2.02) | 0.546 | 4/16 | 25.0 | 0.70 (0.18–2.66) | 0.746 |
| Absent | 34 | 32/34 | 94.1 | 20/34 | 58.8 | 17/34 | 50 | 11/34 | 32.4 | |||||||||
| Fat | Present | 6 | 6/6 | 100 | N/A | 1.000 | 4/6 | 66.7 | 1.26 (0.21–7.64) | 1.000 | 1/6 | 16.7 | 0.20 (0.22–1.854) | 0.199 | 1/6 | 16.7 | 0.43 (0.05–4.02) | 0.654 |
| Absent | 44 | 39/44 | 88.6 | 27/44 | 61.4 | 22/44 | 50 | 14/44 | 31.8 | |||||||||
| Skin and Hair | Present | 6 | 6/6 | 100 | N/A | 1.000 | 4/6 | 66.7 | 1.26 (0.21–7.64) | 1.000 | 0/6 | 0 | N/A | 0.025 | 1/6 | 16.7 | 0.43 (0.05–4.02) | 0.654 |
| Absent | 44 | 39/44 | 88.6 | 27/44 | 61.4 | 23/44 | 52.3 | 14/44 | 31.8 | |||||||||
| Conventional Livestock | Present | 36 | 33/36 | 91.7 | 1.83 (0.27–12.38) | 0.611 | 20/36 | 55.6 | 0.34 (0.08–1.43) | 0.118 | 17/36 | 47.2 | 1.19 (0.34–4.14) | 0.517 | 9/36 | 25.0 | 0.44 (0.12–1.63) | 0.185 |
| Absent | 14 | 12/14 | 85.7 | 11/14 | 78.6 | 6/14 | 42.9 | 6/14 | 42.9 | |||||||||
| Minor Livestock | Present | 14 | 12/14 | 85.7% | 0.55 (0.08–3.67) | 0.611 | 10/14 | 71.4 | 1.79 (0.47–6.79) | 0.522 | 7/14 | 50.0 | 1.25 (0.36–4.31) | 0.761 | 8/14 | 57.1 | 5.52 (1.43–21.14) | 0.016 |
| Absent | 36 | 33/36 | 91.7% | 21/36 | 58.3 | 16/36 | 44.4 | 7/36 | 19.4 | |||||||||
| Wild Animals | Present | 4 | 4/4 | 100 | N/A | 0.647 | 1/4 | 25.0 | 0.18 (0.02–1.85) | 0.147 | 3/4 | 75.0 | 3.90 (0.38–40.37) | 0.246 | 2/4 | 50.0 | 2.54 (0.32–19.96) | 0.346 |
| Absent | 46 | 41/46 | 89.1 | 30/46 | 65.2 | 20/46 | 43.5 | 13/46 | 28.3 | |||||||||
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He, J.; Chantziaras, I.; Garcia-Graells, C.; Ringenier, M.; Dewulf, S.; Boyen, F.; Dewulf, J.; Boland, C. Occurrence of Antimicrobial Resistance in Indicator Bacteria and Campylobacter spp. Isolated from Commercial Raw-Meat-Based Food for Dogs and Cats in Belgium. Antibiotics 2026, 15, 282. https://doi.org/10.3390/antibiotics15030282
He J, Chantziaras I, Garcia-Graells C, Ringenier M, Dewulf S, Boyen F, Dewulf J, Boland C. Occurrence of Antimicrobial Resistance in Indicator Bacteria and Campylobacter spp. Isolated from Commercial Raw-Meat-Based Food for Dogs and Cats in Belgium. Antibiotics. 2026; 15(3):282. https://doi.org/10.3390/antibiotics15030282
Chicago/Turabian StyleHe, Junjia, Ilias Chantziaras, Cristina Garcia-Graells, Moniek Ringenier, Suzanne Dewulf, Filip Boyen, Jeroen Dewulf, and Cécile Boland. 2026. "Occurrence of Antimicrobial Resistance in Indicator Bacteria and Campylobacter spp. Isolated from Commercial Raw-Meat-Based Food for Dogs and Cats in Belgium" Antibiotics 15, no. 3: 282. https://doi.org/10.3390/antibiotics15030282
APA StyleHe, J., Chantziaras, I., Garcia-Graells, C., Ringenier, M., Dewulf, S., Boyen, F., Dewulf, J., & Boland, C. (2026). Occurrence of Antimicrobial Resistance in Indicator Bacteria and Campylobacter spp. Isolated from Commercial Raw-Meat-Based Food for Dogs and Cats in Belgium. Antibiotics, 15(3), 282. https://doi.org/10.3390/antibiotics15030282

